A maize WAK-SnRK1α2-WRKY module regulates nutrient availability to defend against head smut disease

Obligate biotrophs depend on living hosts for nutrient acquisition to complete their lifecycle, yet the mechanisms by which hosts restrict nutrient availability to pathogens remain largely unknown. The fungal pathogen Sporisorium reilianum infects maize seedlings and causes head smut disease in inflorescences at maturity, while a cell wall-associated kinase, ZmWAK, provides quantitative resistance against it. Here, we demonstrate that S. reilianum can rapidly activate ZmWAK kinase activity, which is sustained by the 407th Threonine residue in the juxtamembrane domain, enabling it to interact with and phosphorylate ZmSnRK1α2, a conserved sucrose non-fermenting-related kinase α subunit. The activated ZmSnRK1α2 translocates from the cytoplasm to the nucleus, where it phosphorylates and destabilizes the transcription factor ZmWRKY53. The reduced ZmWRKY53 abundance leads to the downregulation of genes involved in transmembrane transport and carbohydrate metabolism, resulting in nutrient starvation for S. reilianum in the apoplast. Our study uncovers a WAK-SnRK1α2-WRKY53 signaling module in maize that conveys phosphorylation cascades from the plasma membrane to the nuclei to confer resistance against head-smut in maize, with profound implications for crop management and application.